Fumigant toxicity and sublethal effects of Thymus munbyanus essential oil on biomarkers, reproduction, and locomotion in the Mediterranean flour moth Ephestia kuehniella

Authors

  • Zahia C. Hamida Department of Biology, University Badji Mokhtar Annaba, Faculty of Sciences, Applied Animal biology Laboratory, Annaba, Algeria https://orcid.org/0000-0001-7904-1777
  • Hadjira Bendjedid Department of Biology, University Badji Mokhtar Annaba, Faculty of Sciences, Applied Animal biology Laboratory, Annaba, Algeria https://orcid.org/0000-0002-6199-6214
  • Mohamed C. Oulhaci 1. Department of Biology, University Badji Mokhtar Annaba, Faculty of Sciences, Applied Animal biology Laboratory, Annaba, Algeria; 2. Department of Organismal Biology, Faculty of Nature and Life Sciences, Mustefa Ben Boulaïd Batna 2 University, Batna, Algeria https://orcid.org/0009-0007-9637-6377
  • Amina Yezli 1. Department of Biology, University Badji Mokhtar Annaba, Faculty of Sciences, Applied Animal biology Laboratory, Annaba, Algeria; 2. Teacher Education College of Setif, Algeria https://orcid.org/0000-0003-2624-4743
  • Samira Yezli-Touiker Department of Biology, University Badji Mokhtar Annaba, Faculty of Sciences, Applied Animal biology Laboratory, Annaba, Algeria https://orcid.org/0000-0002-1156-2100

DOI:

https://doi.org/10.2298/ABS251229003H

Keywords:

Ephestia kuehniella, Thymus munbyanus, essential oil, fumigant toxicity, biomarker

Abstract

Paper description:

  • Thymus munbyanus essential oil was evaluated as a botanical fumigant for controlling the Mediterranean flour moth, Ephestia kuehniella, a major pest of stored grain products.
  • A range of fumigation concentrations was first tested to determine the lethal doses causing 25% and 50% mortality, which were then used to assess sublethal effects on adult survival and behaviour.
  • Exposure induced oxidative stress responses by increasing glutathione S-transferase and catalase activities, and caused neurotoxicity through acetylcholinesterase inhibition.
  • Reduced mobility and reproductive performance suggest long-term population suppression potential, supporting the development of eco-friendly botanical insecticides.

Abstract: This study evaluated the fumigant toxicity of Thymus munbyanus subsp. coloratus essential oil against adult Ephestia kuehniella (Zeller). To determine sublethal effects, we integrated biochemical biomarkers with assessments of reproductive performance and locomotor activity. Adults were exposed via fumigation to concentrations between 0.05 and 0.8 μL/mL of air, with lethal concentrations calculated after 24 h of exposure. The essential oil showed strong fumigant activity, with LD25 and LD50 values of 0.153 and 0.26 μL/mL of air, respectively. Sublethal exposure at these concentrations was associated with changes in biomarker responses in adults, including increased glutathione S-transferase (GST) and catalase (CAT) activities, along with decreased acetylcholinesterase (AChE) activity. In addition, fumigation affected adult reproductive performance by reducing oviposition, as reflected by a decrease in the number of eggs laid and hatched. Locomotor activity was also impaired, with reductions in distance traveled, movement duration, and movement speed. Overall, these findings suggest that T. munbyanus essential oil has potential as a botanical fumigant against E. kuehniella adults.

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References

Yu J. Chemical Composition of Essential Oils and Their Potential Applications in Postharvest Storage of Cereal Grains. Molecules. 2025;30(3):683. https://doi.org/10.3390/molecules30030683

Elbrense H, El Husseiny I, Abo El Makarem HA, Abo Arab R, El Kholy S. Insecticidal, antifeedant and repellent efficacy of certain essential oils against adult rust-red flour beetle, Tribolium castaneum. Egypt J Chem. 2022;65(1):167-78. https://doi.org/10.21608/ejchem.2021.79263.3897

Bendjedid H, Yezli-touiker S, Taffar A. Yezli A, Souilah N. Impact of Infestation of Flour by Stored Food Pest Insects Ephestia Kuehniella on Quality Flour: Physico-Chemical Analyses. J Bioresour Manag. 2024;11(1):12.

FAO. The four betters and leaving no one behind [Internet]. Rome (IT): Food and Agriculture Organization of the United Nations; 2022 [cited 2025 Dec 1]. Available from: https://www.fao.org/faostat/en/#home

Yezli-Touiker S, Kirane-Amrani L, Meskache R, Soltani N. Effect of captopril on growth development and cuticular secretion in pupae of the Mediterranean flour moth, Ephestia kuehniella Zeller. Fresenius Environ Bull. 2019;28(2):733-8.

Taffar A, Yezli-Touiker S, Bendjedid H, Soltani N. Evaluation of azadirachtin, a biopesticides, on growth, development and cuticle secretion of Mediterranean flour moth, Ephestia kuehniella Zeller. J Entomol Res. 2021;45(3):436-43. https://doi.org/10.5958/0974-4576.2021.00068.2

Kathirvelu C, Maline AS, Sivasankari S. Effect of essential oils as repellent against coleopteran pests of stored produce. J Entomol Res. 2020;44(3):371-6. https://doi.org/10.5958/0974-4576.2020.00063.8

Drabo F, Doumbia S, Sangaré L, Konaté A, Sissoko F, Sanogo Y. Résistance des insectes ravageurs des denrées stockées aux insecticides: cas de Sitophilus zeamais et Tribolium castaneum au Mali. J Appl Biosci. 2019;133:13543-50.

Rezende-Teixeira P, Dusi RG, Jimenez PC, Espindola LS, Costa-Lotufo LV. What can we learn from commercial insecticides? Efficacy, toxicity, environmental impacts, and future developments. Environ Pollut. 2022;300:118983. https://doi.org/10.1016/j.envpol.2022.118983

Gad HA, Al-Anany MS, Atta AA, Al-Ayat AA, Abdelgaleil SA. Efficacy of abamectin and emamectin benzoate alone or in binary combinations with carvone, p-cymene and menthone for the control of Callosobruchus maculatus. J Nat Pestic Res. 2025;11:100106. https://doi.org/10.1016/j.napere.2024.100106

Karabörklü S, Ayvaz A. A comprehensive review of effective essential oil components in stored-product pest management. J Plant Dis Protect. 2023;130(3):449-81. https://doi.org/10.1007/s41348-023-00712-0

Bendif H, Boudjeniba M, Miara MD, Biqiku L, Bramucci M, Caprioli G, Maggi F. Rosmarinus eriocalyx: An alternative to Rosmarinus officinalis as a source of antioxidant compounds. Food chemi. 2017;218:78-88. https://doi.org/10.1016/j.foodchem.2016.09.063

Sadou H, Aouad M, Ghalem S. Chemical composition, antioxidant and antiproliferative activities of essential oil from Thymus munbyanus from Algeria. S Afr J Bot. 2020;130:246-52.

Bendjedid H, Yezli-Touiker S, Taffar A, Soltani N. Phytochemical composition and insecticidal activities of essential oil of Thymus munbyanus (Lamiales: Lamiaceae) aerial parts and its properties against biomarkers of Ephestia kuehniella Zeller (Lepidoptera: Pyralidae). J Essent Oil bear Plants. 2021;24(4):792-807. https://doi.org/10.1080/0972060X.2021.1984315

Pandır D, Baş H. Compositional analysis and toxicity of four plant essential oils to different stages of Mediterranean flour moth, Ephestia kuehniella Zeller (Lepidoptera: Pyralidae). Turk J Entomol. 2016;40(2):185-95. https://doi.org/10.16970/ted.82833

Chapman RF. The insects: structure and function. 5th ed. Cambridge: Cambridge University Press; 2013.

Nation JL. Insect physiology and biochemistry. 4th ed. Boca Raton:CRC Press; 2022.

Regnault-Roger C, Philogène BJR, Vincent C. Biopesticides d'origine végétale. Tropicultura. 2006;24(2):124.

Lee SE. Biochemical mechanisms conferring cross-resistance to fumigant toxicities of essential oils in a chlorpyrifos-methyl resistant strain of Oryzaephilus surinamensis L.(Coleoptera: Silvanidae). J Stored Prod Res. 2002;38(2):157-66. https://doi.org/10.1016/S0022-474X(01)00013-3

Isman MB. "Botanical insecticides, deterrents, and repellents in modern agriculture and an increasingly regulated world. Annu Rev Entomol. 2006;51(1):45-66. https://doi.org/10.1146/annurev.ento.51.110104.151146

Rajendran S, Sriranjini V. Plant products as fumigants for stored-product insect control. Stored Prod Res. 2008;44(2):126-35. https://doi.org/10.1016/j.jspr.2007.08.003

Bostanian NJ, Akalach M, Chiasson H. Effects of a Chenopodium based botanical insecticide/acaricide on Orius insidiosus (Hemiptera: Anthocoridae) and Aphidius colemani (Hymenoptera: Braconidae). Pest Manag Sci. 2005;61:979-84. https://doi.org/10.1002/ps.1065

Ngamo LS, Hance TH. Diversité des ravageurs des denrées et méthodes alternatives de lutte en milieu tropical Tropicultura. 2007;25:215-20.

Yezli-Touiker S, Soltani-Mazouni N. Profil des ecdystéroïdes durant la métamorphose et rapport avec le cycle cuticulaire chez Ephestia kuehniella (Insecta, Lepidoptera, Pyralidae). Synthèse. 2011;22:49-55.

Titouhi F, Amri M, Messaoud C, Haouel S, Youssfi S, Cherif A, Mediouni Ben Jemâa J. Protective effects of three Artemisia essential oils against Callosobruchus maculatus and Bruchus rufimanus (Coleoptera: Chrysomelidae) and the extended side-effects on their natural enemies. J Stored Prod Res. 2017;72:11-20. https://doi.org/10.1016/j.jspr.2017.02.007

Abbott WW. A method for computing the effectiveness of an insecticide. J Econ Entomol.1925;18:265-7. https://doi.org/10.1093/jee/18.2.265a

Habig WH, Pabst MJ, Jackoby WB. Glutathione S-transferases. The first enzymatic step in mercapturic acid formation. J Biol Chem. 1974;249(22):7130-9. https://doi.org/10.1016/S0021-9258(19)42083-8

Claiborne Stephens J, Nei M. Phylogenetic analysis of polymorphic DNA sequences at the Adh locus in Drosophila melanogaster and its sibling species. J Mol Evol. 1985;22(4):289-300. https://doi.org/10.1007/BF02115684

Ellman GL, Courtney KD, Andres Jr V, Featherstone RM. A new and rapid colorimetric determination of acetylcholinesterase activity. Biochem Pharm. 1961;7(2):88-95. https://doi.org/10.1016/0006-2952(61)90145-9

Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem. 1976;72(1-2):248-54. https://doi.org/10.1016/0003-2697(76)90527-3

Polano Ody L, Ferraz AD, de Mello E, Ugalde G, Mazutti, MA, Tres MV, Zabot GL. Trichilia claussenii (Meliaceae): A Review of Its Biological and Phytochemical Activities and a Case Study of Composition. Processes. 2025;13(10):3058. https://doi.org/10.3390/pr13103058

Elbehery HH, Ibrahim SS. Potential fumigant toxicity of essential oils against Sitotroga cerealella (Olivier) (Lepidoptera:Gelechiidae) and its egg parasitoid Trichogramma evanescens (Hymenoptera: Trichogrammatidae). Sci Rep. 2024;14(1):6253. https://doi.org/10.1038/s41598-024-56611-3

Ayvaz A, Sagdic O, Karaborklu S, Ozturk I. Insecticidal activity of the essential oils from different plants against three stored-product insects. J Insect Sci. 2010;10(1):21. https://doi.org/10.1673/031.010.2101

Moazeni N, Khajeali J, Izadi H, Mahdian K. Chemical composition and bioactivity of Thymus daenensis Celak (Lamiaceae) essential oil against two lepidopteran stored-product insects. J Essent Oil Res. 2014; 26(2):118-24. https://doi.org/10.1080/10412905.2013.860412

Mikhaiel AA. Potential of some volatile oils in protecting packages of irradiated wheat flour against Ephestia kuehniella and Tribolium castaneum. J Stored Prod Res. 2011;47(4):357-64. https://doi.org/10.1016/j.jspr.2011.06.002

Ben Chaabene R, Martinez M, Bonavoglia A, Maco B, Chang YW, Lentini G, Soldati-Favre D. Toxoplasma gondii rhoptry discharge factor 3 is essential for invasion and microtubule-associated vesicle biogenesis. PloS Biol. 2024;22(8):e3002745. https://doi.org/10.1371/journal.pbio.3002745

Beshkoufe S, Azizi R, Afrazeh Z, Nemati A, Mojarab-Mahboubkar M, Sendi JJ. The effect of Artemisia annua essential oil and one of its main components on the biology and enzymatic and non-enzymatic activities of Ephestia kuehniella Zeller (Lepidoptra: Pyralidae). Invertebr Survival J. 2025;22(1):64-77.

Ercan F, Baş H, Ercan N, Vural C, Ozcan S. Fumigant toxicitiy of essential oils from Thymus argaeus Boissier & Balansa and Thymus sipyleus Boissier (Lamiaceae) againts Ephestia kuehniella Zeller (Lepidoptera: Pyralidae). Int J Sci Technol Res. 2018;4(3):54-60.

Eltalawy HM, El-Fayoumi H, Aboelhadid SM, Al-Quraishy S, El-Mallah AM, El-Ela FI, Abdel-Baki AA. Insecticidal activity and systematic insights of carvacrol against Tribolium castaneum: Acetylcholinesterase inhibition, oxidative stress, and molecular docking. J Stored Prod Res. 2025;112:102638. https://doi.org/10.1016/j.jspr.2025.102638

Krzyżowski M, Baran B, Łozowski B, Francikowski J. The effect of Rosmarinus officinalis essential oil fumigation on biochemical, behavioral, and physiological parameters of Callosobruchus maculatus. Insects. 2020;11(6):344. https://doi.org/10.3390/insects11060344

Lazarević J, Jevremović S, Kostić I, Vuleta A, Manitašević Jovanović S, Kostić M, Šešlija Jovanović D. Assessment of sex-specific toxicity and physiological responses to thymol in a common bean pest Acanthoscelides obtectus Say. Front Physiol. 2022;13:842314. https://doi.org/10.3389/fphys.2022.842314

Jing TX, Wu YX, Li T, Wei DD, Smagghe GG, Wang JJ. Identification and expression profiles of fifteen delta-class glutathione S-transferase genes from a stored-product pest, Liposcelis entomophila (Enderlein) (Psocoptera: Liposcelididae). Comp Biochem Physiol. 2017;206:35-41. https://doi.org/10.1016/j.cbpb.2017.01.008

Shahriari M, Zibaee A, Mirhaghparast SK, Pour SA, Ramzi S, Hoda H. Mortality and physiological impacts of the tea saponin against Ephestia kuehniella Zeller (Lepidoptera: Pyralidae). Toxin rev. 2022;41(4):1077-85. https://doi.org/10.1080/15569543.2021.1974042

Yezli A, Boudjelida H, Arroussi D. Components and toxicological effects of Myrtus communis L. (myrtales: myrtaceae) essential oil against mosquito Culex pipiens L. (diptera: culicidae). J Appl Ecol. 2024;22(3):2164. https://doi.org/10.15666/aeer/2203_21492164

Ighodaro OM, Akinloye OA. First line defence antioxidants-superoxide dismutase (SOD), catalase (CAT) and glutathione peroxidase (GPX): Their fundamental role in the entire antioxidant defence grid. Alex J Med. 2018;54(4):287-93. https://doi.org/10.1016/j.ajme.2017.09.001

Shahriari M, Zibaee A, Sahebzadeh N, Shamakhi L. Effects of α-pinene, trans-anethole, and thymol as the essential oil constituents on antioxidant system and acetylcholine esterase of Ephestia kuehniella Zeller (Lepidoptera: Pyralidae). Pestic biochem physiol. 2018;150:40-7. https://doi.org/10.1016/j.pestbp.2018.06.015

Wei H, Liu J, Li B, Zhan Z, Chen Y, Tian H, Gu X. The toxicity and physiological effect of essential oil from Chenopodium ambrosioides against the diamondback moth, Plutella xylostella (Lepidoptera: Plutellidae). Crop prot. 2015;76:68-74. https://doi.org/10.1016/j.cropro.2015.06.013

Mojarab-Mahboubkar M, Sendi JJ. Evaluating the potential of Artemisia annua essential oil for controlling Hyphantria cunea (Lepidoptera: Erebidae): effects on larval development, immune function, and enzymatic activities. J Econ Entomol. 2025;118(4):1680-93. https://doi.org/10.1093/jee/toaf120

Farhadi B, Amiri A, Pourabad RF, Bandani AR. Transgenerational effects of peppermint essential oil on life table parameters and antioxidant enzymes in Callosobruchus maculatus. Sci Rep. 2025;15(1):20721. https://doi.org/10.1038/s41598-025-08563-5

Lonare M, Kumar M, Raut S, Badgujar P, Doltade S, Telang A. Evaluation of imidacloprid-induced neurotoxicity in male rats: a protective effect of curcumin. Neurochem Int. 2014;78:122-9. https://doi.org/10.1016/j.neuint.2014.09.004

Jankowska M, Rogalska J, Wyszkowska J, Stankiewicz M. Molecular targets for components of essential oils in the insect nervous system-a review. Molecules. 2017;23(1):34. https://doi.org/10.3390/molecules23010034

Dandlen SA, Miguel MG, Duarte J, Faleiro ML, Sousa MJ, Lima AS, Pedro LG. Acetylcholinesterase inhibition activity of Portuguese Thymus species essential oils. Essent Oil-bear Plant. 2011;14(2):140-50. https://doi.org/10.1080/0972060X.2011.10643914

Rizvi SA, Ling S, Tian F, Xie F, Zeng X. (2018). Toxicity and enzyme inhibition activities of the essential oil and dominant constituents derived from Artemisia absinthium L. against adult Asian citrus psyllid Diaphorina citri Kuwayama (Hemiptera: Psyllidae). Ind Crops Prod. 2018;121:468-75. https://doi.org/10.1016/j.indcrop.2018.05.031

Benelli G, Pavela R, Petrelli R, Cappellacci L, Bartolucci F, Canale A, Maggi F. Origanum syriacum subsp. syriacum: From an ingredient of Lebanese 'manoushe'to a source of effective and eco-friendly botanical insecticides. Ind Crops Prod. 2019;134:26-32. https://doi.org/10.1016/j.indcrop.2019.03.055

Yezli-Touiker S, Soltani-Mazouni N, Kirane-Amrani L, Soltani N. Delayed effects of caproptil on the mediterranean flour moth: reproductive events, of ovaries. Biochemical composition and molting hormone contents of ovaries. Fresen Environ Bull. 2016;25(4):1190-205.

Sabbour MM, Abd El-Aziz SE. Impact of certain nano oils against Ephestia kuehniella and Ephestia cutella (Lepidoptera-Pyralidae) under laboratory and store conditions. Bull Natl Res Cent. 2019;43(1):80. https://doi.org/10.1186/s42269-019-0129-3

Gorji M. Oviposition deterrent effects and ovicidal activity of three species of Iranian endemic savory on Mediterranean flour moth (Ephestia kuehniella Zeller (Lepidoptera: Pyralidae). Iran J Med Aromat Plants Res. 2024;40(2):388-99.

Hossain M.S, Akter S, Hossain M.F, Rizvi S.Z, Mendez V, Taylor P, Park S.J. Essential oils as potential insecticides and behavior-modifying agents against Bactrocera tryoni (Diptera: Tephritidae). J Insect Sci. 2025;25(5):ieaf073. https://doi.org/10.1093/jisesa/ieaf073

Yezli A, Arroussi D.E.R, Boudjelida H, Bensouici C. Repellency and activity evaluation of Myrtus communis essential oil on physiology and reproduction of mosquito species Culex pipiens. Fresen Environ Bull. 2024; 33(5):407-17.

Bayley M. Basic behaviour: The use of animal locomotion in behavioural ecotoxicology. In: Dell'Omo G, editor. Behavioural Ecotoxicology. London, UK: John Wiley; 2002. p 211-30.

Lopes L.M, Sousa A.H, Faroni L.R, Silva M.V, Ferraz M.S, Santos V.B. Toxicity and Sublethal Effects of Piper hispidinervum Essential Oil on Behavioral and Physiological Responses of Sitophilus zeamais Populations. Molecules. 2024;29(17):4116. https://doi.org/10.3390/molecules29174116

Lee S.H, Do H.S, Min K.J. Effects of essential oil from Hinoki cypress, Chamaecyparis obtusa, on physiology and behavior of flies. PloS one. 2015;10(12):e0143450. https://doi.org/10.1371/journal.pone.0143450

Finetti L, Tiedemann L, Zhang X, Civolani S, Bernacchia G, Roeder T. Monoterpenes alter TAR1-driven physiology in Drosophila species. J Exp Biol. 2021;224(1):jeb232116.

Ramin M, Azizi P, Motamedi F, Haghparast A, Khodagholi F. Inhibition of JNK phosphorylation reverses memory deficit induced by β-amyloid (1-42) associated with decrease of apoptotic factors. Behav Brain Res. 2011;217(2):424-31. https://doi.org/10.1016/j.bbr.2010.11.017

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2026-04-09

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Hamida ZC, Bendjedid H, Oulhaci MC, Yezli A, Yezli-Touiker S. Fumigant toxicity and sublethal effects of Thymus munbyanus essential oil on biomarkers, reproduction, and locomotion in the Mediterranean flour moth Ephestia kuehniella. Arch Biol Sci [Internet]. 2026Apr.9 [cited 2026Apr.10];78(1):69-7. Available from: https://www.serbiosoc.org.rs/arch/index.php/abs/article/view/12020

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